Negative frequency-dependent selection underlies overyielding through neighbour genotypic effects in Arabidopsis thaliana

Negative frequency-dependent selection (FDS) can increase both genetic diversity and population-level mean fitness. While the dual consequence of negative FDS has been theoretically recognized, its genomic basis remains unknown. To explore a genetic link between negative FDS and overyielding, I conducted a genome-wide association study (GWAS) of neighbour genotypic effects on the growth of 98 Arabidopsis thaliana genotypes. By incorporating neighbour genotypic similarity, this GWAS analysis detected the most significant single-nucleotide polymorphism (SNP) on the fifth chromosome of A. thaliana, which was 6 kbp from a known locus responsible for indirect genetic effects. I found negative FDS on the most significant SNP, where individual plants increased their biomass in the presence of neighbours with a dissimilar allele. I also observed overyielding in which a biallelic mixture of the most significant SNP showed a 3% increase in biomass compared with monoallelic conditions. Furthermore, I focused on the genomic region near the most significant SNP and found a signature of balancing selection near a negative regulator of ethylene responses, SIRTUIN 2. The present analysis uncovered a quantitative trait locus linking balanced polymorphisms and overyielding in A. thaliana, providing a proof of principle to understand the maintenance of polymorphism and its positive impact on population productivity. This article is part of the theme issue 'Exploring negative frequency-dependent selection across levels: from genetics to ecology and back again'.